Identifying potential evolutionary consequences of climate-driven phenological shifts

Climate change is shifting the phenology of many species throughout the world. While the interspecific consequences of these phenological shifts have been well documented, the intraspecific shifts and their resultant evolutionary consequences remain relatively unexplored. Here, we present a conceptual framework and overview of how phenological shifts within species can drive evolutionary change. We suggest that because the impacts of climate change are likely to vary across the range of a species and differentially impact individuals, phenological shifts may often be highly variable both within and among populations. Together these changes have the potential to alter existing patterns of gene flow and influence evolutionary trajectories by increasing phenological isolation and connectivity. Recent research examining the response of species to contemporary climate change suggests that both phenological isolation and connectivity may be likely responses to future climate change. However, recent studies also show mixed results on whether adaptive responses to climate change are likely to occur, as some populations have already shown adaptive responses to changing climate, while others have not despite fitness costs. While predicting the exact consequences of intraspecific phenological shifts may be difficult, identifying the evolutionary implications of these shifts will allow a better understanding of the effects of future climate change on species persistence and adaptation.     

The importance of phylogeny to the study of phenological response to global climate change

Climate change has resulted in major changes in the phenology—i.e. the timing of seasonal activities, such as flowering and bird migration—of some species but not others. These differential responses have been shown to result in ecological mismatches that can have negative fitness consequences. However, the ways in which climate change has shaped changes in biodiversity within and across communities are not well understood. Here, we build on our previous results that established a link between plant species'' phenological response to climate change and a phylogenetic bias in species'' decline in the eastern United States. We extend a similar approach to plant and bird communities in the United States and the UK that further demonstrates that climate change has differentially impacted species based on their phylogenetic relatedness and shared phenological responses. In plants, phenological responses to climate change are often shared among closely related species (i.e. clades), even between geographically disjunct communities. And in some cases, this has resulted in a phylogenetically biased pattern of non-native species success. In birds, the pattern of decline is phylogenetically biased but is not solely explained by phenological response, which suggests that other traits may better explain this pattern. These results illustrate the ways in which phylogenetic thinking can aid in making generalizations of practical importance and enhance efforts to predict species'' responses to future climate change.     

Marine biological shifts and climate

Phenological, biogeographic and community shifts are among the reported responses of marine ecosystems and their species to climate change. However, despite both the profound consequences for ecosystem functioning and services, our understanding of the root causes underlying these biological changes remains rudimentary. Here, we show that a significant proportion of the responses of species and communities to climate change are deterministic at some emergent spatio-temporal scales, enabling testable predictions and more accurate projections of future changes. We propose a theory based on the concept of the ecological niche to connect phenological, biogeographic and long-term community shifts. The theory explains approximately 70% of the phenological and biogeographic shifts of a key zooplankton Calanus finmarchicus in the North Atlantic and approximately 56% of the long-term shifts in copepods observed in the North Sea during the period 1958–2009.     

How phenological tracking shapes species and communities in non-stationary environments

Climate change alters the environments of all species. Predicting species responses requires understanding how species track environmental change, and how such tracking shapes communities. Growing empirical evidence suggests that how species track phenologically – how an organism shifts the timing of major biological events in response to the environment – is linked to species performance and community structure. Such research tantalizingly suggests a potential framework to predict the winners and losers of climate change, and the future communities we can expect. But developing this framework requires far greater efforts to ground empirical studies of phenological tracking in relevant ecological theory. Here we review the concept of phenological tracking in empirical studies and through the lens of coexistence theory to show why a community-level perspective is critical to accurate predictions with climate change. While much current theory for tracking ignores the importance of a multi-species context, basic community assembly theory predicts that competition will drive variation in tracking and trade-offs with other traits. We highlight how existing community assembly theory can help understand tracking in stationary and non-stationary systems. But major advances in predicting the species- and community-level consequences of climate change will require advances in theoretical and empirical studies. We outline a path forward built on greater efforts to integrate priority effects into modern coexistence theory, improved empirical estimates of multivariate environmental change, and clearly defined estimates of phenological tracking and its underlying environmental cues.     

Phenological responses of plants to climate change in an urban environment

Global climate change is likely to alter the phenological patterns of plants due to the controlling effects of climate on plant ontogeny, especially in an urbanized environment. We studied relationships between various phenophases (i.e., seasonal biological events) and interannual variations of air temperature in three woody plant species (Prunus davidiana, Hibiscus syriacus, and Cercis chinensis) in the Beijing Metropolis, China, based on phenological data for the period 1962–2004 and meteorological data for the period 1951–2004. Analysis of phenology and climate data indicated significant changes in spring and autumn phenophases and temperatures. Changes in phenophases were observed for all the three species, consistent with patterns of rising air temperatures in the Beijing Metropolis. The changing phenology in the three plant species was reflected mainly as advances of the spring phenophases and delays in the autumn phenophases, but with strong variations among species and phenophases in response to different temperature indices. Most phenophases (both spring and autumn phenophases) had significant relationships with temperatures of the preceding months. There existed large inter- and intra-specific variations, however, in the responses of phenology to climate change. It is clear that the urban heat island effect from 1978 onwards is a dominant cause of the observed phenological changes. Differences in phenological responses to climate change may cause uncertain ecological consequences, with implications for ecosystem stability and function in urban environments.     

Phenological plasticity is a poor predictor of subalpine plant population performance following experimental climate change

Phenological shifts, changes in the seasonal timing of life cycle events, are among the best documented responses of species to climate change. However, the consequences of these phenological shifts for population dynamics remain unclear. Population growth could be enhanced if species that advance their phenology benefit from longer growing seasons and gain a pre-emptive advantage in resource competition. However, it might also be reduced if phenological advances increase exposure to stresses, such as herbivores and, in colder climates, harsh abiotic conditions early in the growing season. We exposed subalpine grasslands to ~3 K of warming by transplanting intact turfs from 2000 m to 1400 m elevation in the eastern Swiss Alps, with turfs transplanted within the 2000 m site acting as a control. In the first growing season after transplantation, we recorded species’ flowering phenology at both elevations. We also measured species’ cover change for three consecutive years as a measure of plant performance. We used models to estimate species’ phenological plasticity (the response of flowering time to the change in climate) and analysed its relationship with cover changes following climate change. The phenological plasticity of the 18 species in our study varied widely but was unrelated to their changes in cover. Moreover, early- and late-flowering species did not differ in their cover response to warming, nor in the relationship between cover changes and phenological plasticity. These results were replicated in a similar transplant experiment within the same subalpine community, established one year earlier and using larger turfs. We discuss the various ecological processes that can be affected by phenological shifts, and argue why the population-level consequences of these shifts are likely to be species- and context-specific. Our results highlight the importance of testing assumptions about how warming-induced changes in phenotypic traits, like phenology, impact population dynamics.     

A perspective on match/mismatch of phenology in community contexts

Climate change has significant impacts on phenology of various organisms in a species‐specific manner. Facing this problem, the match/mismatch hypothesis that phenological (a)synchrony with resource availability strongly influences recruitment success of a consumer population has recently received much attention. In this article, we discuss extending the conventional pairwise concept and demonstrate a community module‐based approach as an initial step for exploring community consequences of species‐specific phenological shifts caused by climate change. Our multispecies match/mismatch perspective leads to the prediction that phenological (a)synchrony among interacting species critically affects not only population recruitment of species but also key dynamical features of ecological communities such as trophic cascades, competitive hierarchies, and species coexistence. Explicit identification and consideration of species relationships is therefore desirable for a better understanding of seasonal community dynamics and thus community consequences of climate change‐induced phenological shifts.     

The roles of shifting and filtering in generating community‐level flowering phenology

Plant phenologies are key components of community assembly and ecosystem function, yet we know little about how phenological patterns differ among ecosystems. Community‐level phenological patterns may be driven by the filtering of species into communities based on their phenology or by intraspecific responses to local conditions that shift when species flower. To understand the relative roles of filtering and shifting on community‐level phenological patterns we compared patterns of first flowering dates (FFD) for herbaceous species at Konza Prairie, KS, USA with those from the colder Fargo, ND, USA area and from Chinnor, England, which has a less continental climate. Comparing patterns of FFD supports that Konza's flowering patterns are potentially influenced both by filtering species that flower early in the growing season and by phenological shifting. Konza species flowering dates were earlier in the spring and later in the fall compared to Fargo, but were not shifted compared to Chinnor, which had a unique suite of early‐flowering species. In all, comparing flowering phenology among three sites reveals that intraspecific responses to climate can generate phenological shifts that compress or stretch community‐level phenological patterns, while novel niches in phenological space can also alter community‐level patterns. Community flowering patterns related to climate suggest that climatic warming has the potential to further distribute flowering of the Konza flora over a longer period, but also could further open it to introductions of non‐native species that have evolved to flower early in the season.     

Latitudinal patterns in the phenological responses of leaf colouring and leaf fall to climate change in Japan

Aim  To estimate the potential effect of global climate change on the phenological responses of plants it is necessary to estimate spatial variations at larger scales. However, previous studies have not estimated latitudinal patterns in the phenological response directly. We hypothesized that the phenological response of plants varies with latitude, and estimated the phenological response to long-term climate change using autumn phenological events that have been delayed by recent climate change.
Location  Japan.
Methods  We used a 53-year data set to document the latitudinal patterns in the climate responses of the timing of autumn leaf colouring and fall for two tree species over a wide range of latitudes in Japan (31 to 44° N). We calculated single regression slopes for leaf phenological timing and air temperature across Japan and tested their latitudinal patterns using regression models. The effects of latitude, time and their interaction on the responses of the phenological timings were also estimated using generalized linear mixed models.
Results  Our results showed that single regression slopes of leaf phenological timing and air temperature in autumn were positive at most stations. Higher temperatures can delay the timing of leaf phenology. Negative relationships were found between the phenological response of leaves to temperature and latitude. Single regression slopes of the phenological responses at lower latitudes were larger than those at higher latitudes.
Main conclusions  We found negative relationships between leaf phenological responsiveness and latitude. These findings will be important for predicting phenological timing with global climate change.     

The impact of climate change on birds

Weather is of major importance for the population dynamics of birds, but the implications of climate change have only recently begun to be addressed. There is already compelling evidence that birds have been affected by recent climate changes. This review suggests that although there is a substantial body of evidence for changes in the phenology of birds, particularly of the timing of migration and of nesting, the consequences of these responses for a species' population dynamics is still an area requiring in-depth research. The potential for phenological miscuing (responding inappropriately to climate change, including a lack of response) and for phenological disjunction (in which a bird species becomes out of synchrony with its environment) are beginning to be demonstrated, and are also important areas for further research. The study of climatically induced distributional change is currently at a predictive modelling stage, and will need to develop methods for testing these predictions. Overall, there is a range of intrinsic and extrinsic factors that could potentially inhibit adaptation to climate change and these are a high priority for research.     

Climatic effects on the phenology of lake processes

Populations living in seasonal environments are exposed to systematic changes in physical conditions that restrict the growth and reproduction of many species to only a short time window of the annual cycle. Several studies have shown that climate changes over the latter part of the 20th century affected the phenology and population dynamics of single species. However, the key limitation to forecasting the effects of changing climate on ecosystems lies in understanding how it will affect interactions among species. We investigated the effects of climatic and biotic drivers on physical and biological lake processes, using a historical dataset of 40 years from Lake Washington, USA, and dynamic time‐series models to explain changes in the phenological patterns among physical and biological components of pelagic ecosystems. Long‐term climate warming and variability because of large‐scale climatic patterns like Pacific decadal oscillation (PDO) and El Niño–southern oscillation (ENSO) extended the duration of the stratification period by 25 days over the last 40 years. This change was due mainly to earlier spring stratification (16 days) and less to later stratification termination in fall (9 days). The phytoplankton spring bloom advanced roughly in parallel to stratification onset and in 2002 it occurred about 19 days earlier than it did in 1962, indicating the tight connection of spring phytoplankton growth to turbulent conditions. In contrast, the timing of the clear‐water phase showed high variability and was mainly driven by biotic factors. Among the zooplankton species, the timing of spring peaks in the rotifer Keratella advanced strongly, whereas Leptodiaptomus and Daphnia showed slight or no changes. These changes have generated a growing time lag between the spring phytoplankton peak and zooplankton peak, which can be especially critical for the cladoceran Daphnia. Water temperature, PDO, and food availability affected the timing of the spring peak in zooplankton. Overall, the impact of PDO on the phenological processes were stronger compared with ENSO. Our results highlight that climate affects physical and biological processes differently, which can interrupt energy flow among trophic levels, making ecosystem responses to climate change difficult to forecast.     

Avian Community Responses to Variability in River Hydrology

River flow is a major driver of morphological structure and community dynamics in riverine-floodplain ecosystems. Flow influences in-stream communities through changes in water velocity, depth, temperature, turbidity and nutrient fluxes, and perturbations in the organisation of lower trophic levels are cascaded through the food web, resulting in shifts in food availability for consumer species. River birds are sensitive to spatial and phenological mismatches with aquatic prey following flow disturbances; however, the role of flow as a determinant of riparian ecological structure remains poorly known. This knowledge is crucial to help to predict if, and how, riparian communities will be influenced by climate-induced changes in river flow characterised by more extreme high (i.e. flood) and/or low (i.e. drought) flow events. Here, we combine national-scale datasets of river bird surveys and river flow archives to understand how hydrological disturbance has affected the distribution of riparian species at higher trophic levels. Data were analysed for 71 river locations using a Generalized Additive Model framework and a model averaging procedure. Species had complex but biologically interpretable associations with hydrological indices, with species’ responses consistent with their ecology, indicating that hydrological-disturbance has implications for higher trophic levels in riparian food webs. Our quantitative analysis of river flow-bird relationships demonstrates the potential vulnerability of riparian species to the impacts of changing flow variability and represents an important contribution in helping to understand how bird communities might respond to a climate change-induced increase in the intensity of floods and droughts. Moreover, the success in relating parameters of river flow variability to species’ distributions highlights the need to include river flow data in climate change impact models of species’ distributions.     

Phylogenetic conservatism and climate factors shape flowering phenology in alpine meadows

The study of phylogenetic conservatism in alpine plant phenology is critical for predicting climate change impacts; currently we have a poor understanding of how phylogeny and climate factors interactively influence plant phenology. Therefore, we explored the influence of phylogeny and climate factors on flowering phenology in alpine meadows. For two different types of alpine plant communities, we recorded phenological data, including flowering peak, first flower budding, first flowering, first fruiting and the flowering end for 62 species over the course of 5 years (2008–2012). From sequences in two plastid regions, we constructed phylogenetic trees. We used Blomberg’s K and Pagel’s lambda to assess the phylogenetic signal in phenological traits and species’ phenological responses to climate factors. We found a significant phylogenetic signal in the date of all reproductive phenological events and in species’ phenological responses to weekly day length and temperature. The number of species in flower was strongly associated with the weekly day lengths and followed by the weekly temperature prior to phenological activity. Based on phylogenetic eigenvector regression (PVR) analysis, we found a highly shared influence of phylogeny and climate factors on alpine species flowering phenology. Our results suggest the phylogenetic conservatism in both flowering and fruiting phenology may depend on the similarity of responses to external environmental cues among close relatives.     

Tell me what you eat and I'll tell you when you fly: diet can predict phenological changes in response to climate change

Changes in phenology are correlated with climate change. However, we still struggle to understand the traits making species susceptible to climate change, and the implications of species' reactions for communities and food webs. Butterflies and moths are an ecologically important group that have shown pronounced phenological changes over the last decades. Tests using a > 150-year dataset from 566 European butterfly and moth species demonstrated that variation in phenological change was strongly related to traits describing plant-herbivore interactions (larval diet breadth, diet composition), and the life cycle. The results indicate that climate change related shifts in phenology are correlated with the seasonal availability and palatability of food plants. Lepidopterans feeding on herbaceous plants showed smaller shifts in flight periods but larger increases in voltinism than lepidopterans feeding on woody plants. Consequently, the effect of herbivorous lepidopterans may increase in herb-rich grassland ecosystems under warmer conditions, and not in forest ecosystems.     

Elevational trends in butterfly phenology: implications for species responses to climate change

1. Impacts of global change on the distribution, abundance, and phenology of species have been widely documented. In particular, recent climate change has led to widespread changes in animal and plant seasonality, leading to debate about its potential to cause phenological mismatches among interacting taxa. 2. In mountainous regions, populations of many species show pronounced phenological gradients over short geographic distances, presenting the opportunity to test for effects of climate on phenology, independent of variation in confounding factors such as photoperiod. 3. Here we show for 32 butterfly species sampled for five years over a 1700 m gradient (560–2260 m) in a Mediterranean mountain range that, on average, annual flight period is delayed with elevation by 15–22 days per kilometre. Species mainly occurring at low elevations in the region, and to some extent those flying earlier in the year, showed phenological delays of 23–36 days per kilometre, whereas the flight periods of species that occupy high elevations, or fly in late summer, were consistently more synchronised over the elevation gradient. 4. Elevational patterns in phenology appear to reflect a narrowing phenological window of opportunity for larval and adult butterfly activity of high elevation and late‐flying species. 5. Here, we speculate as to the causes of these patterns, and the consequences for our ability to predict species responses to climate change. Our results raise questions about the use of space–time substitutions in predicting phenological responses to climate change, since traits relating to flight period and environmental associations may influence the capacity of species to adapt to changing climates.     

Forecasting phenology under global warming

As a consequence of warming temperatures around the world, spring and autumn phenologies have been shifting, with corresponding changes in the length of the growing season. Our understanding of the spatial and interspecific variation of these changes, however, is limited. Not all species are responding similarly, and there is significant spatial variation in responses even within species. This spatial and interspecific variation complicates efforts to predict phenological responses to ongoing climate change, but must be incorporated in order to build reliable forecasts. Here, we use a long-term dataset (1953–2005) of plant phenological events in spring (flowering and leaf out) and autumn (leaf colouring and leaf fall) throughout Japan and South Korea to build forecasts that account for these sources of variability. Specifically, we used hierarchical models to incorporate the spatial variability in phenological responses to temperature to then forecast species'' overall and site-specific responses to global warming. We found that for most species, spring phenology is advancing and autumn phenology is getting later, with the timing of events changing more quickly in autumn compared with the spring. Temporal trends and phenological responses to temperature in East Asia contrasted with results from comparable studies in Europe, where spring events are changing more rapidly than are autumn events. Our results emphasize the need to study multiple species at many sites to understand and forecast regional changes in phenology.     

The impact of altered precipitation variability on annual weed species

? Premise of the study: Climate change models predict increasing variability in precipitation across the globe, with an increase in the incidence of large precipitation events but decreasing overall event frequency. Research with annual species in arid and semiarid ecosystems has demonstrated that precipitation variability can influence plant community dynamics; however, less is known about the impact of precipitation variability in less water-limited ecosystems, including economically important agricultural systems. ? Methods: We conducted three greenhouse experiments to determine how variation in total precipitation and the interval between precipitation events affected emergence and growth of two common annual midwestern weed species, Chenopodium album (Chenopodiaceae) and Setaria faberi (Poaceae). ? Key results: Both species responded to precipitation variability; however, the effect depended on life stage and precipitation amount, indicating that responses are highly context-dependent. Emergence of both species increased with longer intervals between precipitation events at low total precipitation, but species' responses varied under typical precipitation amounts. Individual seedling biomass of both species depended on interactions between total water and intervals, but species' responses differed; Setaria faberi biomass was reduced with longer intervals, but Chenopodium album had either a positive or no response. ? Conclusions: Our results suggest that changes in precipitation variability likely will affect the composition and relative abundance of agriculturally important weeds. These results are important for understanding how changes in the temporal variability of precipitation due to global climate changes could impact plants in non-arid communities.     

Disentangling the paradox of insect phenology: are temporal trends reflecting the response to warming?

The strength and direction of phenological responses to changes in climate have been shown to vary significantly both among species and among populations of a species, with the overall patterns not fully resolved. Here, we studied the temporal and spatial variability associated with the response of several insect species to recent global warming. We use hierarchical models within a model comparison framework to analyze phenological data gathered over 40 years by the Japan Meteorological Agency on the emergence dates of 14 insect species at sites across Japan. Contrary to what has been predicted with global warming, temporal trends of annual emergence showed a later emergence day for some species and sites over time, even though temperatures are warming. However, when emergence data were analyzed as a function of temperature and precipitation, the overall response pointed out an earlier emergence day with warmer conditions. The apparent contradiction between the response to temperature and trends over time indicates that other factors, such as declining populations, may be affecting the date phenological events are being recorded. Overall, the responses by insects were weaker than those found for plants in previous work over the same time period in these ecosystems, suggesting the potential for ecological mismatches with deleterious effects for both suites of species. And although temperature may be the major driver of species phenology, we should be cautious when analyzing phenological datasets as many other factors may also be contributing to the variability in phenology.     

A 250-year index of first flowering dates and its response to temperature changes

Widespread concerns about global biodiversity loss have led to a growing demand for indices of biodiversity status. Today, climate change is among the most serious threats to global biodiversity. Although many studies have revealed phenological responses to climate change, no long-term community-level indices have been developed. We derived a 250-year index of first flowering dates for 405 plant species in the UK for assessing the impact of climate change on plant communities. The estimated community-level index in the most recent 25 years was 2.2–12.7 days earlier than any other consecutive 25-year period since 1760. The index was closely correlated with February–April mean Central England Temperature, with flowering 5.0 days earlier for every 1°C increase in temperature. The index was relatively sensitive to the number of species, not records per species, included in the model. Our results demonstrate how multi-species, multiple-site phenological events can be integrated to obtain indices showing trends for each species and across species. This index should play an important role in monitoring the impact of climate change on biodiversity. Furthermore, this approach can be extended to incorporate data from other taxa and countries for evaluating cross-taxa and cross-country phenological responses to climate change.     

The dynamics of climate-induced range shifting; perspectives from simulation modelling

Predicted future climate change will alter species' distributions as they attempt to track the most suitable 'climate window'. Climate envelope models indicate the direction of likely range changes but do not incorporate population dynamics, therefore observed responses may differ greatly from these projections. We use simulation modelling to explore the consequences of a period of environmental change for a species structured across an environmental gradient. Results indicate that a species' range may lag behind its climate envelope and demonstrate that the rate of movement of a range can accelerate during a period of climate change. We conclude that the inclusion of both population dynamics and spatial environmental variability is vital to develop models that can both predict, and be used to manage, the impact of changing climate on species' biogeography.